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LETTERS TO THE EDITOR

there was no association, although an inverse association was found in the model without adjustment for BMI on the basis of only 2 studies. Given the findings above, limited evidence supports the inverse association between nut consumption and risk of type 2 diabetes. None of the authors had a conflict of interest.

Zhihao Liu Jiangsu Provincial Center for Disease Prevention and Control 172 Jiangsu Road Nanjing China E-mail: [email protected]

Southeast University of China Nanjing China Xiaoning Li Jiangsu Provincial Center for Disease Prevention and Control 172 Jiangsu Road Nanjing China Note: Afshin et al chose not to submit a reply.

REFERENCES 1. Zhou D, Yu H, He F, Reilly KH, Zhang J, Li S, Zhang T, Wang B, Ding Y, Xi B. Nut consumption in relation to cardiovascular risk and type 2 diabetes: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr 2014;100:270–7. 2. Luo C, Zhang Y, Ding Y, Shan Z, Chen S, Yu M, Hu FB, Liu L. Nut consumption and risk of type 2 diabetes, cardiovascular disease, and allcause mortality: a systematic review and meta-analysis. Am J Clin Nutr 2014;100:256–69. 3. Afshin A, Micha R, Khatibzadeh S, Mozaffarian D. Consumption of nuts and legumes and risk of incident ischemic heart disease, stroke, and diabetes: a systematic review and meta-analysis. Am J Clin Nutr 2014;100:278–88. 4. Montonen J, Jarvinen R, Heliovaara M, Reunanen A, Aromaa A, Knekt P. Food consumption and the incidence of type II diabetes mellitus. Eur J Clin Nutr 2005;59:441–8. 5. Parker ED, Harnack LJ, Folsom AR. Nut consumption and risk of type 2 diabetes. JAMA 2003;290:38–9; author reply 39–40. 6. Pan A, Sun Q, Manson JE, Willett WC, Hu FB. Walnut consumption is associated with lower risk of type 2 diabetes in women. J Nutr 2013;143:512–8.

doi: 10.3945/ajcn.114.093302.

Sleep duration and energy intake: timing matters Dear Sir: It was with great interest that we read the article by Kant and Graubard (1). The authors examined both self-reported sleep duration and eating patterns of ;15,000 adult Americans of the NHANES

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Pingmin Wei

cohort. The main finding was that short sleepers, ie, those reporting sleeping 6 h/night, were found to consume breakfast earlier and consume fewer main meals but more snacks compared with average sleepers (habitual sleep duration between 7 and 8 h). In contrast, self-reported eating behavior did not differ between average and long sleepers (ie, 9 h). Finally, the overall self-reported 24-h energy intake was not different between short, average, and long sleepers. Notwithstanding their elegant demonstration of the association between short sleep and altered eating patterns, Kant and Graubard did not investigate whether short sleepers also eat at times of the day when the circadian system is not metabolically adjusted to process ingested nutrients or stimulants such as caffeine (ie, primarily during the night). Indeed, their article does not report how many of those who were self-reported short sleepers were also shift workers. This is an important aspect of the analysis of food intake in relation to sleep and circadian timing, because shift workers are often forced to eat, and not only sleep, at odd times of their 24-h day, including during the night (2), times during which the body is more insulin resistant and generally disadvantageously adapted to handling food intake. Not only did previous studies link shift work with the development of obesity but they also showed that under conditions of experimental circadian disruption, in which sleep is misaligned in much the same way as experienced by many shift workers, this alters the hormonal profile, increases inflammation, and reduces insulin sensitivity (3, 4). Hormones responsible for determining the appetitive and metabolic response to food intake, such as the hunger-promoting hormone ghrelin and the satiety-enhancing adipokine leptin, are known to be perturbed by circadian misalignment (4, 5). Although with ad libitum food intake such paradigms can lead to increased food intake, circadian misalignment can even promote weight loss under apparently isocaloric conditions, ie, if food intake is equal between groups, matched to the calculated 24-h energy expenditure (5). In an intervention aiming for weight loss, the timing at which food intake occurs was also linked to the success of weight loss (6), such that late lunch eaters lost less weight than did early lunch eaters during the 20-wk intervention. At the molecular level, when the circadian machinery was disrupted in mice due to genetic mutation of the gene Clock, this resulted in obesity (7). Forcing wild-type mice under ad libitum high-fat diet conditions to flip their circadian eating time by 12 h, effectively eating during their ‘‘physiological’’ night, led to a 48% increase in body weight, as opposed to a 20% increase for the mice with a normal meal pattern (8). Importantly, these differences were noted despite no significant differences in energy intake between the 2 groups of mice. Importantly, if food is provided at the incorrect time of day, this may in the long run not only cause an increase in body weight but also predispose individuals to develop type 2 diabetes—the risk of which a recent meta-analysis once more confirmed to be elevated for individuals who perform shift work (9). The importance of circadian misalignment for such ultimate consequences of shift work was highlighted by the fact that workers with rotating shifts, in which the timing of both sleep and food intake will keep occurring at time points to which the body cannot adapt to quickly enough from a chronobiological viewpoint, had the highest risk of developing type 2 diabetes. Shift work, or the experimental version thereof, with desynchronizing extended sleepwake cycles or day lengths (2, 3, 9), are known to lead to reduced average sleep duration and sleep quality. Although Kant and Graubard did not find any differences in after-dinner meals between short, average, or long sleepers, they found a higher percentage of 24-h energy intake at or after 2000 h in short sleepers (1). This suggests that this sleep group may still consume significant amounts of energy at inappropriate time

LETTERS TO THE EDITOR points of the day (ie, night), perhaps in combination with metabolically equally challenging mistimed sleep. Given that eating at the ‘‘wrong’’ time from a circadian perspective may increase the risk of weight gain, even under neutral energy balance conditions, an important next step would be to examine to what extent specifically misaligned sleep or rotating sleep schedules—habits typically seen in those who ‘‘work on shifts’’—favor energy surplus and metabolic consequences in cohorts such as NHANES. The authors’ work is supported by the Novo Nordisk Foundation, Swedish ˚ ke Wiberg Foundation. The authors are unaware of Brain Foundation, and A any affiliation, funding, or financial holdings that might be perceived as affecting the objectivity of this letter to the editor.

Department of Neuroscience Uppsala University Box 593 751 24 Uppsala Sweden E-mail: [email protected]

REFERENCES 1. Kant AK, Graubard BI. Association of self-reported sleep duration with eating behaviors of American adults: NHANES 2005–2010. Am J Clin Nutr (Epub ahead of print 23 July 2014). 2. Lowden A, Moreno C, Holmba¨ck U, Lennerna¨s M, Tucker P. Eating and shift work—effects on habits, metabolism and performance. Scand J Work Environ Health 2010;36:150–62. 3. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA 2009;106:4453–8. 4. Leproult R, Holmba¨ck U, Van Cauter E. Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes 2014;63:1860–9. 5. Buxton OM, Cain SW, O’Connor SP, Porter JH, Duffy JF, Wang W, Czeisler CA, Shea SA. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci Transl Med 2012;4(129):129ra43. 6. Garaulet M, Go´mez-Abella´n P, Alburquerque-Be´jar JJ, Lee YC, Ordova´s JM, Scheer FA. Timing of food intake predicts weight loss effectiveness. Int J Obes (Lond) 2013;37:604–11. 7. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005;308:1043–5. 8. Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW. Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 2009;17:2100–2. 9. Gan Y, Yang C, Tong X, Sun H, Cong Y, Yin X, Li L, Cao S, Dong X, Gong Y, et al. Shift work and diabetes mellitus: a meta-analysis of observational studies. Occup Environ Med 2014 Jul 16 (Epub ahead of print; DOI:10.1136/oemed-2014-102150). doi: 10.3945/ajcn.114.096875.

Reply to J Cedernaes and C Benedict Dear Sir: We appreciate Cedernaes and Benedict’s interest in our recent work on eating behaviors in relation to duration of sleep (1). The

focus of the letter by Cedernaes and Benedict is metabolic and health concerns due to disruption of circadian eating and sleeping norms in shift work, a promising area of study, which was not the subject of our article. In their summary of findings of our study, Cedernaes and Benedict state that ‘‘self-reported eating behavior did not differ between average and long sleepers (ie, 9 h).’’ Our article makes no such assertions. In fact, both tabular and narrative results show that many eating behaviors of long-duration sleepers were similar to those of short-duration sleepers but different from average-duration sleepers (eg, less likely to report breakfast, less energy from main meals, more energy from snacks, etc). These findings are also mentioned in the Discussion. Cedernaes and Benedict also state that we did not examine ‘‘whether short sleepers also eat at times of the day when the circadian system is not metabolically adjusted to process ingested nutrients or stimulants such as caffeine (ie, primarily during the night).’’ Our study addressed this question in at least 3 ways by examination of the following: 1) the percentage of 24-h energy that was reported at or after 2000 h (shown in our Table 2), 2) the number of snack episodes (and % of energy) reported after dinner by dinner reporters (shown in our Table 3), and 3) the clock time of the last reported eating episode of the recalled day (shown in our Table 4). Short-duration sleepers did report modestly higher energy intakes at or after 2000 h and a later time of the last eating episode of the day. Last, we want to emphasize that the exposure in our study was hours of self-reported weekday/workday nighttime sleep. During our preliminary analyses we found employment status (yes or no) to be a correlate of sleep duration as well as of energy intake and eating behaviors. Hence, all reported analyses in the article were adjusted for employment status. It is unlikely that additional control for shift work will alter our findings. Overall, in our analytic sample, 10.87% (95% CI: 10.13%, 11.65%) of adult Americans reported evening/night/rotating work schedules. The prevalences (sample weighted %) of evening, night, and rotating work schedules in short-, average-, and long-duration sleepers were 13.45% (12.19%, 14.82%), 9.20% (8.34%, 10.14%), and 10.78% (7.92%, 14.51%), respectively. The multiple variable–adjusted mean hours of sleep reported by regular day schedule reporters (6.82 h; 95% CI: 6.77, 6.87 h) were not significantly different from those of evening/night/ rotating schedule reporters (6.76 h; 95% CI: 6.65, 6.88 h). Mean hours of sleep reported by nonemployed Americans, however, were higher at 7.01 h (95% CI: 6.94, 7.08 h) and significantly different from those who worked day or evening/night/rotating schedules. Interestingly, in the NHANES 2007–2008, the metabolic profiles (eg, BMI, waist circumference, serum triglycerides, LDL cholesterol, and glycated hemoglobin) of Americans reporting evening/night/rotating work schedules did not differ from those of regular day shift workers (2). Nevertheless, to address the concern about possible confounding of sleep duration and eating behavior association by shift work, we conducted further sensitivity analyses. We repeated analyses for key eating behavior outcomes after exclusion of evening/night/rotating shift reporters from the analytic sample and after addition of a variable to indicate evening/night/rotating schedule to the regression models. With both approaches, as shown in Table 1, the substantive findings of our study were unchanged. The review by Lowden et al (3), also cited by Cedernaes and Benedict, found the available evidence on the association of shift work and eating to be ‘‘complex’’ and ‘‘contradictory.’’ Thus, we look forward to more research on norms of circadian rhythms of eating and sleeping behaviors and individual adaptations to dyssynchrony resulting from constraints of work and leisure in

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Jonathan Cedernaes Christian Benedict

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Sleep duration and energy intake: timing matters.

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